We study the dynamics of the adaptation of cardiac energy metabolism to metabolic demand. The goal is to understand the regulation of cardiac energy metabolism and its effects on heart function in health and disease. To this end the time course of oxygen uptake in the heart is derived from measurements in the coronary venous effluent, usually during step changes in demand, and deconvoluted with the mitochondrial-to-venous transport function resulting in the time course of the response of mitochondrial oxygen consumption to changes in ATP hydrolysis. Lactate output and content of high-energy phosphates (using 31P-NMR spectroscopy) are also experimentally determined in a time-resolved way. We found that the "time constant" of mitochondrial oxygen consumption after steps in metabolic demand was about 8 s at 37 degrees Celsius. The time constant increased by 110% per 10 degrees Celsius decrease in temperature, and was 2-3 times slower when intracellular pH was lowered by 0.6. Mitochondrial capacity was a strong determinant of the time constant at low heart rates, but not at high heart rates. The response was faster when the intramitochondrial dehydrogenase activity was increased. The time constant of the phosphate metabolites determined with NMR spectroscopy was shorter than of oxygen consumption. This means that there is a gap in the balance of ATP synthesis and hydrolysis which we explain by a brief burst of glycolytic ATP production. However, lactate must stay intracellularly since we do not find a peak in lactate efflux after a step in heart rate. We model cardiac energy metabolism with a linearized non- equilibrium thermodynamic model in which mitochondria are regulated via the cytosolic phosphorylation potential, and also with enzyme-kinetic models. These simple models enabled us to explain the time constant of oxygen consumption, the effect of temperature and the effect of cytosolic acidification.